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Open Access Research article

Differential gene expression and metabolomic analyses of Brachypodium distachyon infected by deoxynivalenol producing and non-producing strains of Fusarium graminearum

Jean-Claude Pasquet1, Séjir Chaouch1, Catherine Macadré1, Sandrine Balzergue2, Stéphanie Huguet2, Marie-Laure Martin-Magniette23, Floriant Bellvert4, Xavier Deguercy1, Vincent Thareau1, Dimitri Heintz5, Patrick Saindrenan1 and Marie Dufresne1*

Author Affiliations

1 Institut de Biologie des Plantes, Unité Mixte de Recherche 8618, Saclay Plant Sciences, Université Paris-Sud, Orsay 91405, France

2 INRA/CNRS/UEVE – URGV, Saclay Plant Sciences, 2, rue Gaston Crémieux, CP5708, Evry cedex 91057, France

3 INRA-AgroParisTech, MIA 518, 16 rue Claude Bernard, Paris Cedex 75005, France

4 Laboratoire d'Ingénierie des Systèmes Biologiques et des Procédés – INSA, UMR INSA/CNRS 5504 - UMR INSA/INRA 792, 135 Avenue de Rangueil, Toulouse cedex 4 31077, France

5 Institut de Biologie Moléculaire des Plantes, Unité Propre de Recherche du CNRS, UPR 2357, Plateforme Métabolomique, 28 rue Goethe, Strasbourg 67083, France

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BMC Genomics 2014, 15:629  doi:10.1186/1471-2164-15-629

Published: 25 July 2014

Abstract

Background

Fusarium Head Blight (FHB) caused primarily by Fusarium graminearum (Fg) is one of the major diseases of small-grain cereals including bread wheat. This disease both reduces yields and causes quality losses due to the production of deoxynivalenol (DON), the major type B trichothecene mycotoxin. DON has been described as a virulence factor enabling efficient colonization of spikes by the fungus in wheat, but its precise role during the infection process is still elusive. Brachypodium distachyon (Bd) is a model cereal species which has been shown to be susceptible to FHB. Here, a functional genomics approach was performed in order to characterize the responses of Bd to Fg infection using a global transcriptional and metabolomic profiling of B. distachyon plants infected by two strains of F. graminearum: a wild-type strain producing DON (FgDON+) and a mutant strain impaired in the production of the mycotoxin (FgDON-).

Results

Histological analysis of the interaction of the Bd21 ecotype with both Fg strains showed extensive fungal tissue colonization with the FgDON+ strain while the florets infected with the FgDON- strain exhibited a reduced hyphal extension and cell death on palea and lemma tissues. Fungal biomass was reduced in spikes inoculated with the FgDON- strain as compared with the wild-type strain. The transcriptional analysis showed that jasmonate and ethylene-signalling pathways are induced upon infection, together with genes encoding putative detoxification and transport proteins, antioxidant functions as well as secondary metabolite pathways. In particular, our metabolite profiling analysis showed that tryptophan-derived metabolites, tryptamine, serotonin, coumaroyl-serotonin and feruloyl-serotonin, are more induced upon infection by the FgDON+ strain than by the FgDON- strain. Serotonin was shown to exhibit a slight direct antimicrobial effect against Fg.

Conclusion

Our results show that Bd exhibits defense hallmarks similar to those already identified in cereal crops. While the fungus uses DON as a virulence factor, the host plant preferentially induces detoxification and the phenylpropanoid and phenolamide pathways as resistance mechanisms. Together with its amenability in laboratory conditions, this makes Bd a very good model to study cereal resistance mechanisms towards the major disease FHB.

Keywords:
Fusarium Head Blight; Brachypodium distachyon; Transcriptome; Metabolic profiling; Serotonin